Robotically-induced hallucination triggers subtle changes in brain network transitions.

Journal: NeuroImage
Published Date:

Abstract

The perception that someone is nearby, although nobody can be seen or heard, is called presence hallucination (PH). Being a frequent hallucination in patients with Parkinson's disease, it has been argued to be indicative of a more severe and rapidly advancing form of the disease, associated with psychosis and cognitive decline. PH may also occur in healthy individuals and has recently been experimentally induced, in a controlled manner during fMRI, using MR-compatible robotics and sensorimotor stimulation. Previous neuroimaging correlates of such robot-induced PH, based on conventional time-averaged fMRI analysis, identified altered activity in the posterior superior temporal sulcus and inferior frontal gyrus in healthy individuals. However, no link with the strength of the robot-induced PH was observed, and such activations were also associated with other sensations induced by robotic stimulation. Here we leverage recent advances in dynamic functional connectivity, which have been applied to different psychiatric conditions, to decompose fMRI data during PH-induction into a set of co-activation patterns that are tracked over time, as to characterize their occupancies, durations, and transitions. Our results reveal that, when PH is induced, the identified brain patterns significantly and selectively increase their transition probabilities towards a specific brain pattern, centred on the posterior superior temporal sulcus, angular gyrus, dorso-lateral prefrontal cortex, and middle prefrontal cortex. This change is not observed in any other control conditions, nor is it observed in association with other sensations induced by robotic stimulation. The present findings describe the neural mechanisms of PH in healthy individuals and identify a specific disruption of the dynamics of network interactions, extending previously reported network dysfunctions in psychotic patients with hallucinations to an induced robot-controlled specific hallucination in healthy individuals.

Authors

  • Herberto Dhanis
    Center for Neuroprosthetics, Ecole Polytechnique Fédérale de Lausanne, EPFL, Geneva, Switzerland; Brain Mind Institute, Faculty of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland; Institute of Bioengineering, Ecole Polytechnique Fédérale de Lausanne, Lausanne Switzerland; Department of Radiology and Medical Informatics, University of Geneva, Geneva Switzerland.
  • Eva Blondiaux
    Laboratory of Cognitive Neuroscience, Center for Neuroprosthetics & Brain Mind Institute, Ecole Polytechnique Fédérale de Lausanne (EPFL), 1202 Geneva, Switzerland.
  • Thomas Bolton
    Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom.
  • Nathan Faivre
    Laboratory of Cognitive Neuroscience, Center for Neuroprosthetics & Brain Mind Institute, Ecole Polytechnique Fédérale de Lausanne (EPFL), 1202 Geneva, Switzerland.
  • Giulio Rognini
    Center for Neuroprosthetics, Swiss Federal Institute of Technology (EPFL), Geneva, Switzerland; Laboratory of Cognitive Neuroscience, Brain Mind Institute, Faculty of Life Sciences, Swiss Federal Institute of Technology (EPFL), Geneva, Switzerland; Laboratory of Robotic Systems, School of Engineering, Swiss Federal Institute of Technology (EPFL), Lausanne, Switzerland. Electronic address: giulio.rognini@epfl.ch.
  • Dimitri Van De Ville
    Neuro-X Institute, Ecole Polytechnique Fédérale De Lausanne (EPFL), Geneva, Switzerland.
  • Olaf Blanke
    Center for Neuroprosthetics, Swiss Federal Institute of Technology (EPFL), Geneva, Switzerland; Laboratory of Cognitive Neuroscience, Brain Mind Institute, Faculty of Life Sciences, Swiss Federal Institute of Technology (EPFL), Geneva, Switzerland; Department of Neurology, University Hospital of Geneva, Geneva, Switzerland. Electronic address: olaf.blanke@epfl.ch.